Staphylococcus lugdunensis Skin Infection: Report of 16 Cases

ARTICLE IN PRESS +Model ACTAS De mo-Sifiliog áficas xxx (xxxx) xxx---xxx BRIEF COMMUNICATION S aphylococcus lugdunensis Skin In ec ion: Repo o 16 Cases夽 A.J. Ga cía-Malinis,a,∗A. Milag o,bL. To es Sopena,cY. Gilabe ed aUnidad de De ma ología, Hospi al San Jo ge, Huesca, Spain bSe icio de Mic obiología, Hospi al Uni e si a io Miguel Se e , Za agoza, Spain cSe icio de Mic obiología, Hospi al San Jo ge, Huesca, Spain dSe icio de De ma ología, Hospi al Uni e si a io Miguel Se e , Za agoza, Spain KEYWORDS S aphylococcus lugdunensis; Coagulase-nega i e s aphylococci; Skin in ec ion Abs ac In oduc ion and objec i e: S aphylococcus lugdunensis belongs o he g oup o coagulase- nega i e s aphylococci. The aim o his epo was o e iew he clinical and mic obiologic ea u es o cases o S. lugdunensis skin in ec ions. Ma e ial and me hods: Obse a ional s udy o all cases o skin in ec ions in which S. lugdunen- sis was isola ed by he mic obiology depa men o Hospi al Gene al San Jo ge in Huesca, Spain, be ween 2009 and 2016. Resul s: We s udied he cases o 16 pa ien s. The mos equen si e o in ec ion was he inguinal-pe ineal egion (n = 6, 37.5%), and pus ules we e he mos common p esen a ion (n = 5, 31.3%). Response o ea men was good in 87.6% o he pa ien s (n = 14). Howe e , in ec ion ecu ed in 3 pa ien s, 2 o whom we e on an i-TNF he apy. Conclusions: S. lugdunensis should be conside ed a possible cause o in ec ion when i is isola ed in bo h skin and subcu aneous issues, especially in pa ien s on biologic he apies. © 2020 AEDV. Published by Else ie Espa˜ na, S.L.U. This is an open access a icle unde he CC BY-NC-ND license (h p://c ea i ecommons.o g/licenses/by-nc-nd/4.0/). PALABRAS CLAVE S aphylococcus lugdunensis; Es afilococo coagulasa nega i e; In ección cu ánea In ección cu ánea po S aphylococcus lugdunensis: p esen ación de 16 casos Resumen In oducción y obje i o: S aphylococcus lugdunensis pe enece al g upo de los es afilococos coagulasa nega i os. El obje i o del es udio es e isa las ca ac e ís icas clínicas y mic obiológ- icas de los pacien es diagnos icados de una in ección cu ánea po S. lugdunensis. Ma e ial y mé odos: Es udio obse acional e ospec i o de odos los casos de in ecciones cu áneas en las que se aisló S. lugdunensis diagnos icados en e 2009 y 2016 en el Se icio de Mic obiología del Hospi al San Jo ge de Huesca. 夽Please ci e his a icle as: Ga cía-Malinis AJ, Milag o A, To es Sopena L, Gilabe e Y. In ección cu ánea po S aphylococcus lugdunensis: p esen ación de 16 casos. Ac as De mosifiliog . 2020. h ps://doi.o g/10.1016/j.ad.2019.05.017 ∗Co esponding au ho . E-mail add ess: [email p o ec ed] (A.J. Ga cía-Malinis). 1578-2190/© 2020 AEDV. Published by Else ie Espa˜ na, S.L.U. This is an open access a icle unde he CC BY-NC-ND license (h p:// c ea i ecommons.o g/licenses/by-nc-nd/4.0/). ADENGL-2497; No. o Pages 5 ARTICLE IN PRESS +Model A.J. Ga cía-Malinis, A. Milag o, L. To es Sopena e al. Resul ados: Se incluye on 16 pacien es. La localización más ecuen e ue la zona inguinope - ineal (n = 6, 37,5%) y la o ma de p esen ación más habi ual ue on las pús ulas (n = 5, 31,3%). El 87,6% de los pacien es (n = 14) mos a on buena espues a al a amien o; sin emba go, 3 pacien es ecu ie on. De ellos, 2 es aban en a amien o con un an i-TNF. Conclusión: S. lugdunensis debe ía conside a se el posible agen e causal de la in ección cuando se aísla an o en piel como en ejido celula subcu áneo, especialmen e en pacien es que es án ecibiendo a amien o biológico. © 2020 AEDV. Publicado po Else ie Espa˜ na, S.L.U. Es e es un a ´ ıculo Open Access bajo la licencia CC BY-NC-ND (h p://c ea i ecommons.o g/licenses/by-nc-nd/4.0/). In oduc ion S aphylococcus lugdunensis belongs o he g oup o coagulase-nega i e s aphylococci (CoNS). Fi s desc ibed in 1988 by F eney in Lyon, F ance,1 his eme ging pa hogen is mo e i ulen han o he CoNS and can cause in ec ions wi h high mo ali y.2 S lugdunensis is a commensal CoNS in a eas wi h apoc ine glands,3and causes in ec ions o he skin and subcu a- neous cell issue, gene ally esul ing in abscess o ma ion.4 Pa ien s wi h p edisposing condi ions such as diabe es o umo s a e a g ea e isk o acqui ing S lugdunensis in ec- ion, al hough deep and supe ficial in ec ions ha e also been desc ibed in heal hy indi iduals,5in which he skin is he main poin o en y. In his s udy we sough o e iew he clinical and mic o- biological cha ac e is ics o pa ien s in ou cen e who we e diagnosed wi h skin in ec ions om which S lugdunensis was isola ed, as well as he ea men s applied and he cou se o he in ec ion. Ma e ial and Me hods We pe o med a e ospec i e obse a ional s udy o all cases o skin in ec ions o which mic obiological cul u e e ealed he p esence o S lugdunensis a he Mic obiology Se ice o Hospi al San Jo ge de Huesca be ween 2009 and 2016. The ollowing a iables we e eco ded: age; sex; asso- cia ed sys emic diseases and hei ea men ; loca ion and ype o skin lesion; ea men and e olu ion; and o he mic oo ganisms concomi an ly isola ed om he same lesion. Mic obiological diagnosis was based on cul u e o he samples in s anda d media. Mic oo ganism iden ifica ion and an ibio ic sensi i i y es s we e pe o med using Mic oScan® (Beckman Coul e ), applying he c i e ia o he Clinical and Labo a o y S anda ds Ins i u e (CLSI). Iden ifica ion was confi med using he o ni hine deca boxylase (ODC) es and he py olidonyl-a ylamidase (PYR) es (Rosco Diagnos ica A/S, Denma k). Resul s Table 1 summa izes he cha ac e is ics o he sample pop- ula ion, which consis ed o 16 pa ien s (9 women, 7 men) wi h a mean age o 52.19 yea s ( ange, 19---83 y). Six pa ien s (37.5%) had unde lying sys emic diseases. The mos commonly a ec ed loca ion was he inguinal/pe ineal a ea (n = 6, 37.5%), ollowed by he lowe ex emi ies (n = 3, 18.8%). The mos common clinical p esen a ions we e pus ules (n = 5, 31.3%), in e igo- ype lesions (n = 5, 31.3%), and abscessed cys s (n = 3, 18.8%) (Fig. 1A). The p esence o an abscess was epo ed in only 1 pa ien . S lugdunensis was he only pa hogen isola ed in cul u es om 11 (68.8%) o he 16 pa ien s. The mic oo ganism mos equen ly isola ed concomi an ly wi h S lugdunensis was Esche ichia coli (n = 2, 12.5%). A cu ious ea u e o he S lug- dunensis samples isola ed on blood aga was a cha ac e is ic smell o cu ed po k. An an ibiog am pe o med o all samples e ealed an ibio ic sensi i i y o all S lugdunensis isola es, excep o one ha showed esis ance o clindamycin, e y h omycin, os omycin, and e acycline. Fungal cul u e was pe o med in 6 pa ien s, 5 o whom had suspec ed in e igo. O al ea men , he mos common o which was o al penicillin, was ecei ed by 75% o pa ien s (n = 12). Top- ical ea men was ecei ed by 56.3% (n = 9) o pa ien s, o whom 5 ecei ed associa ed o al an ibio ic ea men . Mupi ocin (n = 3, 18.8%) and e y h omycin (n = 2, 12.5%) we e he mos equen ly p esc ibed opical an ibio ics among pa ien s who ecei ed opical ea men . O he 5 pa ien s wi h in e igo-like lesions, only one p esen ed coin ec ion (wi h Candida albicans and T ichophy on ub um), which esponded adequa ely o o al e binafine. In cases in ol ing abscesses o abscessed cys s, he lesions we e d ained. A good ea men esponse was obse ed in 87.6% o pa ien s (n = 14). Two pa ien s, bo h o whom had E coli coin- ec ions, did no espond o ea men . Th ee pa ien s who showed a good ini ial esponse expe ienced ecu ence (2 episodes each). O hese 3 pa ien s, 2 we e being ea ed wi h an i- umo nec osis ac o (TNF) agen s. Discussion Despi e o ming pa o he skin mic obio a, S lugdunensis is o g ea pa hogenic impo ance and, like S aphylococcus au eus, can cause in asi e, highly i ulen communi y and nosocomial in ec ions.6 In ou se ies, skin in ec ions caused by S lugdunen- sis we e mos ly mild and p edominan ly a ec ed he inguinal/pe ineal a ea. The mos equen clinical p esen- 2 ARTICLE IN PRESS +Model ACTAS De mo-Sifiliog áficas xxx (xxxx) xxx---xxx Table 1 Clinical Cha ac e is ics, Coin ec ion S a us, T ea men , and In ec ion Cou se Case Age, y Sex Lesion Loca ion Lesion Type Associa ed Diseases Biological T ea men Concomi an In ec ions O al T ea men Topical T ea men T ea men Response 1 83 Female Lowe limbs Pus ules Diges i e mas ocy o- sis No Co ynebac e ium s ia- um/amycola um Cloxacillin No Good esponse 2 45 Male Abdomen Su gical wound No No No Amoxicillin Mupi ocin Good esponse 3 38 Female Lowe limbs In e igo No No Candida albicans and T ichophy on ub um Te binafine No Good esponse 4 79 Male Inguinal/pe ineal and glu eal egions P essu e ulce No No E coli Amoxicillin Mupi ocin No esponse 5 68 Female Inguinal/pe ineal and glu eal egions Abscess Pso iasis Yes No Doxycycline Fusidic acid and be ame hasone Good ini ial esponse, subsequen ecu ence 6 40 Female Lumba egion Abscessed cys No No No Cloxacillin No Good esponse 7 45 Female Inguinal/pe ineal and glu eal egions Pus ules Hid adeni is No No Clindamycin No Good ini ial esponse, subsequen ecu ence 8 19 Male Inguinal/pe ineal and glu eal egions Pus ules Hid adeni is No No Clindamycin and i ampicin No Good esponse 9 40 Female Abdomen Pus ules Rheuma oid a h i is Yes No Amoxicillin- cla ulanic acid No Good ini ial esponse, subsequen ecu ence 10 53 Male Lumba egion Abscessed cys No No No Cloxacillin No Good esponse 11 41 Male Inguinal/pe ineal and glu eal egions In e igo Hepa i is A i us No S ep ococcus agalac iae (g oup B) No E y h omycin Good esponse 12 61 Male Lowe limbs Pus ules No No No Cloxacillin Mupi ocin Good esponse 13 67 Female Inguinal/pe ineal and glu eal egions In e igo No No No No E y h omycin Good esponse 14 65 Female Submamma y egion In e igo No No No No Fusidic acid Good esponse 15 35 Female Ches Abscessed cys No No No Amoxicillin- cla ulanic acid Fusidic acid and be ame hasone Good esponse 16 56 Male Axillae In e igo No No E coli No Hyd oco isone and miconazole No esponse 3 ARTICLE IN PRESS +Model A.J. Ga cía-Malinis, A. Milag o, L. To es Sopena e al. Figu e 1 A, Abscess caused by S lugdunensis in he inguinal egion o a pa ien ecei ing adalimumab ea men . B, S lugdunensis colony g owing on blood aga . a ions we e in e igo-like and pus ula lesions. Recu ence was obse ed only in pa ien s ea ed wi h an i-TNF agen s. The majo i y o S lugdunensis in ec ions epo ed in he li e a u e p esen as in ec ions o he skin o subcu aneous issue ha esul in abscess o ma ion.7,8 Among 29 cases ecen ly desc ibed by Zaa ou a e al,9 he mos equen p esen a ion was pus ulosis/ olliculi is (16 pa ien s). In line wi h hose findings, pus ules and in e igo we e he mos common p esen a ions (5 cases o each) in ou se ies. The mos equen ly a ec ed loca ions in ou s udy popula ion coincided wi h hose epo ed in p e ious s ud- ies. These include he inguinal/pe ineal a ea,7,10 abdomen, lowe ex emi ies,11 and mamma y egion,5all o which a e a eas in which S lugdunensis is a commensal mic oo ganism. Skin in ec ions due o S lugdunensis usually espond o an ibio ic ea men .11 Unlike o he CoNS, S lugdunensis is gene ally sensi i e o penicillins owing o i s low le els o be a-lac amase p oduc ion, and less han 5% o isola es a e esis an o oxacillin.5In cases o simple skin abscesses, he apeu ic guidelines ecommend incision and d ainage o he lesion; fi s -line an ibio ic ea men is no indica ed. In complica ed cases, d ainage and o al ea men wi h na ow-spec um an ibio ics such as ce ad oxil, cephalexin, o cloxacillin is ecommended. In cases o olliculi is, he d ugs o choice a e mupi ocin and usidic acid, combined wi h hygiene measu es. In pa ien s wi h ex ensi e olliculi- is, addi ion o an o al an ibio ic (ce ad oxil, cephalexin, o cloxacillin) is ecommended.12 The mos common ea - men epo ed in he li e a u e is opical an ibio ic he apy, combined wi h o al an ibio ics in mo e complica ed cases.13 Because S lugdunensis colonizes he skin, i is impo - an o de e mine when his mic oo ganism becomes a pa hogen. One o he cases in ou se ies was a pa ien wi h T ub um and C albicans coin ec ion who esponded a o - ably o e binafine. This is a clea example o S lugdunensis me ely ac ing as a colonizing agen . Co-in ec ion wi h E coli was de ec ed in he 2 pa ien s in which no ea men esponse was obse ed, sugges ing ha E coli, and no S lug- dunensis, was he pa hogen esponsible o he in ec ion. The pa hogenic capaci y o S lugdunensis in os eoa icula in ec ions has been co obo a ed p ospec i ely.14 Howe e , cau ion is ad ised when in e p e ing single posi i e samples om skin o subcu aneous issue o om known niches o his CoNS.15 S lugdunensis in ec ion ha esponded well o an ibio ic ea men has been desc ibed in a pa ien wi h pso iasis and pso ia ic a h i is who was being ea ed wi h adali- mumab and me ho exa e.16 In ou se ies, 2 o he pa ien s who expe ienced lesion ecu ence we e being ea ed wi h an an i-TNF agen , specifically adalimumab. One o he pa ien s swi ched o adalimumab a e showing a poo esponse o an ibio ic ea men . Skin in ec ion is one o he mos equen ly epo ed side e ec s o an i-TNF d ugs.17 This is because TNF-␣ is a p o-inflamma o y cy osine ha plays an impo an ole in inna e immuni y, and he e o e i s inhibi ion can inc ease he isk o in ec ions, especially hose o bac e ial o igin.18 S lugdunensis can be easily iden ified in he labo a o y, p o ided ha i s possible p esence is aken in o conside a- ion. Incuba ion on blood aga o 18 o 24 hou s gi es ise o colonies wi h weak ␤-hemolysis, which inc eases a e 48 hou s (Fig. 1B). Two es s a e equi ed o iden i y his bac e ium: he ODC and PYR es s. Bo h a e posi i e in he case o S lugdunensis, unlike o he CoNS. Ma ix-assis ed lase deso p ion ioniza ion--- ime o fligh mass spec ome y (MALDI-TOF MS) p o ides a apid and cos -e ec i e means o iden i ying S lugdunensis.19 I has a sensi i i y and specifici y close o 100% o he iden ifica ion o CoNS, especially S lugdunensis.20 The p esen se ies was pe o med be o e he ecen acquisi ion o a MALDI-TOF sys em by ou hospi al. The des uc i e na u e o S lugdunensis, i s g ea i u- lence, and i s abili y o cause suppu a i e in ec ions mo e han jus i y ac i e su eillance o his mic oo ganism. In he pas S lugdunensis was occasionally iden ified as a causal agen o human pa hology, bu is now de ec ed wi h inc eas- ing equency. This may be due o be e unde s anding o i s mic obiological cha ac e is ics, a highe index o clini- cal suspicion, and he use o MALDI-TOF, which has enabled cha ac e iza ion o nume ous CoNS species ha we e p e i- ously iden ified simply as coagulase-nega i e s aphylococci o S aphylococcus species.5 S lugdunensis can be conside ed a pa hogenic mic oo - ganism o skin in ce ain ci cums ances, depending on he clinical pic u e and a ec ed loca ion, and in pa ien s wi h sys emic o local isk ac o s, such as hose in ou se ies who we e ea ed wi h an i-TNF agen s. Funding This s udy did no ecei e specific unding om any public sec o , p i a e sec o , o nonp ofi en i ies. 4 ARTICLE IN PRESS +Model ACTAS De mo-Sifiliog áficas xxx (xxxx) xxx---xxx Conflic s o In e es The au ho s decla e ha hey ha e no conflic s o in e es . Re e ences 1. F eney J, B un Y, Bes M, Meugnie H, G imon F, G imon PAD, e al. S aphylococcus lugdunensis sp. no . and S aphylococcus schlei e i sp. no ., wo Species om Human Clinical Specimens. In J Sys E ol Mic obiol. 1988;38:168---72. 2. Yeh C-F, Chang S-C, Cheng C-W, Lin J-F, Liu T-P, Lu J-J. Clinical ea u es, ou comes, and molecula cha ac e - is ics o communi y- and heal h ca e-associa ed S aphylo- coccus lugdunensis in ec ions. J Clin Mic obiol. 2016;54: 2051---7. 3. Böche S, Tønning B, Sko RL, P ag J. S aphylococcus lugdunen- sis, a common cause o skin and so issue in ec ions in he communi y. J Clin Mic obiol. 2009;47:946---50. 4. an de Mee-Ma que N, Acha d A, Me eghe i L, Dan on A, Minie M, Quen in R. S aphylococcus lugdunensis in ec ions: high equency o inguinal a ea ca iage. J Clin Mic obiol. 2003;41:1404---9. 5. Papape opoulos N, Papape opoulou M, Van a akis A. Abscesses and wound in ec ions due o S aphylococcus lugdunensis: epo o 16 cases. In ec ion. 2013;41:525---8. 6. Ce cenado E. [S aphylococcus lugdunensis: a unique coagulase- nega i e s aphylococcus]. En e m In ecc Mic obiol Clin. 2009;27:139---42. 7. Bellamy R, Ba kham T. S aphylococcus lugdunensis in ec ion si es: p edominance o abscesses in he pel ic gi dle egion. Clin In ec Dis. 2002;35:E32---34. 8. Held Manica LA, Cohen PR. Cu aneous S aphylococcus lug- dunensis in ec ion: an eme ging bac e ial pa hogen. De ma ol Online J. 2018;24. 9. Zaa ou a H, Ge en Y, Be gman R, A i an-He sh E. Clinical and mic obiological p ope ies o S aphylococcus lugdunensis skin in ec ions. J De ma ol. 2018;45:994---9. 10. Vandenesch F, Eykyn SJ, E ienne J, Lemozy J. Skin and pos - su gical wound in ec ions due o S aphylococcus lugdunensis. Clin Mic obiol In ec . 1995;1(2):73---4. 11. A ias M, Tena D, Apellániz M, Asensio MP, Caballe o P, He nández C, e al. Skin and so issue in ec ions caused by S aphylo- coccus lugdunensis: epo o 20 cases. Scand J In ec Dis. 2010;42:879---84. 12. Fe nández U usuno R (coo d.). G upo de T abajo de la Guía. Guía de e apéu ica an imic obiana del Á ea Alja a e, 3.a ed, Se illa: Dis i o Sani a io Alja a e-Se illa No e y Hospi al San Juan de Dios del Alja a e; 2018, pp. 207-220. [Accessed 05 Ma 2019]. A ailable in: h p://www.jun adeandalucia. es/se icioandaluzdesalud/guia e apeu icaalja a e/guiaTe a peu icaAlja a e/. 13. Lozano-Masdemon B, Gómez-Recue o-Mu˜ noz L, Pulido-Pé ez A. S aphylococcus lugdunensis: an eme ging pa hogen in skin and so issue in ec ions. Ac as De mosifiliog . 2015;106:769---70. 14. A gemi X, P é os G, Riegel P, Kelle D, Meye N, Baldey ou M, e al. VISLISI ial, a p ospec i e clinical s udy allowing iden ifica ion o a new me allop o ease and pu a i e i ulence ac o om S aphylococcus lugdunensis. Clin Mic obiol In ec . 2017;23:334.e1---8. 15. A gemi X, Hansmann Y, Riegel P, P é os G. Is S aphylococ- cus lugdunensis significan in clinical samples? J Clin Mic obiol. 2017;55:3167---74. 16. Held Manica LA, Cohen PR. S aphylococcus lugdunensis in ec- ions o he skin and so issue: a case se ies and e iew. De ma ol The . 2017;7:555---62. 17. Flend ie M, Visse s WHPM, C eeme s MCW, de Jong EMGJ, an de Ke kho PCM, an Riel PLCM. De ma ological condi ions du ing TNF-alpha-blocking he apy in pa ien s wi h heuma oid a h i- is: a p ospec i e s udy. A h i is Res The . 2005;7:R666---676. 18. Be na sky S, Habel Y, Rahme E. Obse a ional s udies o in ec- ions in heuma oid a h i is: a me aanalysis o umo nec osis ac o an agonis s. J Rheuma ol. 2010;37:928---31. 19. Pa el R. Ma ix-assis ed lase deso p ion ioniza ion- ime o fligh mass spec ome y in clinical mic obiology. Clin In ec Dis. 2013;57:564---72. 20. A gemi X, Riegel P, La igne T, Le eb e N, G andp é N, Hansmann Y, e al. Implemen a ion o ma ix-assis ed lase des- o p ion ioniza ion- ime o fligh mass spec ome y in ou ine clinical labo a o ies imp o es iden ifica ion o coagulase- nega i e s aphylococci and e eals he pa hogenic ole o S aphylococcus lugdunensis. J Clin Mic obiol. 2015;53:2030---6. 5